Karst Environment

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Zeitschrift für Geomorphologie, Vol. 60 (2016), Suppl. 2, 103-117 Article103 published in print June 2016 Karst environment

Karst environment

David C. Culver

with 2 figures and 4 tables

Abstract. Karst environments can be grouped into three broad categories, based on their vertical position in the landscape. Th ere are surface habitats, ones exposed to light; there are shallow subterranean (aphotic) habitats oft en with small to intermediate sized spaces; there are deep subterranean habitats (caves) with large sized spaces. Faunal records are most complete for caves, and on a global basis, more than 10,000 species are limited to this habitat. Hundreds of other species, especially bats, depend on caves for some part of their life cycle. A large, but most unknown number of species are limited to shallow subterranean habitats in karst, such as epikarst and the milieu souterrain superfi ciel. Species in both these categories of habitats typically show a number of morphological adaptations for life in darkness, including loss of eyes and pigment, and elaboration of extra-optic sensory structures. Surface habitats, such as sinkholes, karst springs, thin soils, and rock faces, are habitats, but not always recognized as karst habitats. Both aphotic karst habitats and twilight habitats (such as open air pits) may serve as important temporary refuges for organisms avoiding temperature extremes on the surface.

Key words: Adaptation, biodiversity, caves, climate refuges, shallow subterranean habitats, stygobionts, troglobionts

1 Overview of karst habitats

Because of the process of dissolution of bedrock, karst presents a series of habitats typically not found anywhere else, habitats generally characterized by the absence of light, and usually by the absence of autotrophic food production. Th e best known of these habitats are caves, not strictly limited to karst landscapes (e.g., lava fl ows sometimes called “pseudokarst”(Eberhard & Sharples 2013)), but predominately occurring in karst. Th eir depth ranges from a few meters below the surface, the situation at cave entrances but also for many relatively long passages to several km below the surface, such as Krubera Cave in Georgia (Abkhazia), more than 2 km below the earth’s surface (Klimchouk 2012). Even deeper cavities occur (Dublyansky 2012), but are unexplored biologically. Th e living spaces for organisms are typically of large dimension, on the order of meters, much larger than the organisms themselves. Culver & Pipan (2008, 2011, 2014) analyze subterranean habitats in karst (and other environments) that are close to the surface yet aphotic. In these habitats, the living spaces for organisms are oft en at the same size range as the organisms themselves. Th e action of dissolution of bedrock creates of course not only subsurface features but surface features as well. Th ese surface features, sinkholes, springs, open air pits, and rock faces provide unique habitats for plants and animals.

DOI: 10.1127/zfg_suppl/2016/00306 eschweizerbart_xxx 0372-8854/16/00306 $ 3.75 104 D.C. Culver

1.1 Classifi cation of subterranean habitats by vertical position

From a biological point a view, the key environmental parameter that defi nes subterranean habitats is absence of light. Th e complete absence of light is a formidable barrier to successful colonization (Jeffery 2009, Pipan & Culver 2012), and unites all aphotic environments, resulting in shared morphology (especially eye and pigment loss) by many of its inhabitants. Shallow subterranean habitats diff er from deep subterranean habitats in having greater environmental variability (and cyclicity) and greater fl uxes of organic carbon and nutrients (Culver & Pipan 2014). Although environmental constancy has oft en been emphasized by speleobiol- ogists, especially from North America, even deep caves are typically environmentally variable. Many decades ago, Hawes (1939) emphasized the annual cycle of fl ooding. It is an important cautionary tale that alteration of the fl ow of the Trebišnjica River, which previously fl ooded Vjetrenica (Lučić 2012), a cave in Bosnia & Hercegovina that Hawes studied, had a major deleterious eff ect on the fauna of caves in the area (Čučković 1983, Culver & Pipan 2009), including Vjetrenica.

1.2 Classifi cation of subterranean habitats by habitat size

In his comprehensive compendium of the obligate subterrannean fauna in aquatic habitats, Botosaneanu (1986) distinguished two main types of subterranean habitats – large cavity habitats, especially caves, and small cavity habitats, especially the habitats between gravels or even grains of sand, collectively referred to as interstitial habitats. Both types of habitats occur in karst because small cavity habitats occur in the underfl ow of rivers and streams in karst, both above ground and below ground. Both harbor many species specialized for and limited to subterranean habitats – stygobionts. Stygobionts in the two habitat types typically share the morphological features of reduced eyes and pigment, but diff er in their size. Interstitial species tend to be mini- aturized relative to cave species. An equivalent dichotomy of subterranean habitat types can be described for terrestrial habitats. In this case, the soil takes the place of aquatic interstitial habitats. Th e soil fauna is not nor- mally considered as part of the subterranean fauna (e.g., Sket 2008), but it should be because it is both an aphotic environment and contains species without eyes or pigment (Culver & Pipan 2014). Th e large-small dichotomy of Botosaneanu (1986) is inadequate for several reasons. First and foremost it fails to take into account the range of subterranean habitats, especially those with eyeless and pigmentless species. Th ere are a number of aphotic habitats that have features and commonalities not captured by the large-small dichotomy – ones that we collectively call shallow (superfi cial) subterranean habitats, or SSHs (Culver & Pipan 2008, 2009, 2011, Pipan & Culver 2012). Th ese are subterranean habitats very close to the surface (using the arbitrary cutoff of 10 m), but are also intermediate in habitat size. Th ese habitats include talus and scree slopes. Th e name milieu souterrain superfi cial (MSS), originally used by Juberthie et al. (1980) refers to ero- sional features like scree that are covered with soil or moss. Whatever name is used, it is an SSH with intermediate sized space with many close connections with the surface. Several SSHs occur

eschweizerbart_xxx Karst environment 105 in karst. Epikarst, the uppermost layer of karst formed largely by solution processes (Gabrovšek 2004) that may at any given time be air or water fi lled, occupies a similar vertical position to that of the MSS, but perhaps with smaller spaces. Calcrete aquifers are rather bizarre shallow aquifers formed under arid conditions by evaporation along a length of river draining into a salt lake. In some areas of Western Australia, the only region where they have been studied biologically, they are always less than 10 m deep (Yilgarn) but in others they are typically deeper (Pilbara). Th ese habitats are extensively reviewed by Culver & Pipan (2014).

2 Fauna of caves and other deep subterranean habitats

Th e most extensive data on cave inhabitants covers two quite diff erent groups. One group com- prises the species limited to caves and spend their entire life cycle in caves – aquatic stygobionts and terrestrial troglobionts. Th is fauna is of special interest for at least two reasons. Th e fi rst is the highly convergent, even bizarre morphology of many stygobionts and troglobionts, including eye and pigment loss, appendage elongation, and elaboration of extra-optic sensory structures. Th e iconic cave salamander of the Dinaric karst, Proteus anguinus, epitomizes this morphology (Fig. 1). Th ese convergent morphologies and the evolutionary processes that resulted in them make caves important evolutionary laboratories (Poulson & White 1969). Th e second reason the stygobiotic and troglobiotic fauna is of special interest is its high level of endemism. For example, over half of the stygobionts and troglobionts known from caves east of the Mississippi River in the U.S. are known from a single county, with an average area of 2500 km2 (Christman & Culver 2001). Because of their geographic rarity, most stygobionts and troglobionts are at some level of risk of extinction.

Fig. 1. Th e Dinaric cave salamander Proteus angujinus (photo by Gregor Aljančič, Laboratory Tular).

eschweizerbart_xxx 106 D.C. Culver

Th e second faunal group in caves, for which large amounts of data are available, are bats. Many bats use caves for hibernacula, maternity colonies, and day roosts (Kunz et al. 2012). Bats are of special interest both because of the ecosystem services they provide, including insect con- trol and pollination (Kunz et al. 2011), and because of their susceptibility to large scale extirpa- tion when concentrated in caves and their susceptibility to disease such as white nose syndrome in North America (Moore & Kunz 2012).

2.1 Th e transitory cave fauna

Animals are in subterranean habitats for a variety of reasons. Some may be there by chance or accident. Chapman (1993) describes the odd behavior of Heleomyza fl ies in British caves. Th ey arrive in the autumn and remain in a semi-torpid state for months, many eventually dying from starvation or pathogenic fungi. Of course, a variety of animals blunder into caves, perhaps escap- ing summer heat, and the list of mammals that do so is quite large, including domesticated animals such as sheep and wild animals such as foxes, wolves, and even elephants in African caves. Some of these blunderers end up as a nutrient not as a resident. Some animals occupy caves for part of the day, the best known example being bats that utilize caves in the summer as a day roost. For example, Brazilian free-tailed bat, Tadarida brasiliensis, is present in many caves in the southwestern United States and Mexico in summer months (Barbour & Davis 1969). It uses caves as shelters and places to avoid predators and summer heat during the day while it sleeps and then exits the cave at night to forage for insects. Many other mammals use caves as their shelter. Th e European dormouse, Glis glis, utilizes caves in this way, regularly exiting the cave at night to forage (Tvrtkovič 2005). Th e Allegheny wood rat, Neotoma magister, uses eastern North American caves in a similar way. Invertebrates, including cave-crickets in many North American caves, also enter and exit caves on a regular, oft en daily basis (Lavoie et al. 2007). Many bat species utilize caves in one way or another. Th ese include day roosts, courtship and mating sites, maternity roosts, and hibernacula (Kunz et al. 2012). Nearly half of all genera of bats use caves; the main genera are listed in Table 1. Many temperate zone bats in the families Verspertilionidae, Rhinolophidae, and Molossidae form large hibernating colonies. Among the largest of these are the hibernacula of the endangered North American gray bat Myotis grisescens. Tens of thousands of bats congregate in a few deep, vertical caves with cold air traps (Barbour & Davis 1969). In addition to day roosts and hibernacula, bats also use caves for large maternity roosts, something M. grisescens also does. M. grisescens is one of the most cave dependent bats in the world, using caves throughout the year, although not the same caves in diff erent seasons. It forms large maternity roosts in caves diff erent from the hibernating caves. Perhaps the most spectacular case of mammals using caves to hibernate is the extinct Euro- pean cave bear Ursus spelaeus (Kurtén 1968). Many skeletons of the cave bear are preserved in the Slovenian cave, Križna jama and in the Romanian cave, PeşteraUrşilor. At least in desert environments hyenas (Hyaena hyaena) enter caves to avoid temperature extremes and to eat large scavenged prey (Kempe et al. 2006). Frogs and many invertebrates also over-winter in caves. For example, the moths Scoliopterix libatrix and Triphosa species over-winter in caves throughout

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Europe and North America (Chapman 1993, Graham 1968). Many other arthropods, including Diptera and Opiliones, also over-winter but this phenomenon has been little studied.

2.2 Th e permanent cave fauna

Stygobionts and troglobionts have been found on all continents except Antarctica. Estimates of the number of described species of stygobionts are given in Table 2. Europe dominates the list with 2000 described species. Th e list is incomplete because it is several years out of date, many

Table 1. Bat genera that frequently occupy caves. From Wolszym (1998).

Sub-order Family Genera found in Caves Megachiroptera Pteropidae Banionycteris Eonycteris Penthetor Rousettus Microchiroptera Rhinopomatidae Rhinopoma Emballonuridae Taphozous Craseonycteridae Craseonycteris Rhinolophidae Rhinolophus Hipposideridae Hipposiderus Noctilionidae Noctilio Mormoopidae Pteronotus Phyllostomatidae Artibeus Brachyphylla Erophylla Macrotus Phyllonycteris Vespertilionidae Barbastella Eptesicus Miniopterus Myotis Nycticeius Pipistrellus Plecotus Molossidae Cheiromeles Sauromys Tadarida Nycteridae Nycteris

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Table 2. Estimates of the number of described species of stygobionts from the six continents. From Gibert & Culver (2009).

Continent Number of Stygobionts Europe 2000 Asia 561 Africa 335 North America 500 South America 200 Oceania 226

species have been collected that are not yet described, and most importantly, equal sampling eff ort has not been devoted to each continent. For all continents, the number in Table 2 are but a small fraction of the total number of stygobiotic species. No such estimates are available for troglobionts, which typically outnumber stygobionts (a factor of two in the case of the U.S. cave fauna, Culver et al. 2000). Because of the high levels of endemism, the obligate cave fauna of nearby localities diff ers, and it is diffi cult to obtain an adequate estimate of regional diversity. Such estimates require extensive sampling of caves in a region. Culver et al. (2006) did the broadest such study to date, analyzing the troglobiotic fauna of seven regions of 2000 km2 to 6300 km2 in Europe and North America, each with more 120 caves and 350 records of troglobionts. Supplementing these data with less complete information from 16 other similarly sized areas, they found a ridge (ca 42° to 46° in Europe and 34° in North America) of high biodiversity that coincides in areas of high productivity and cave density. Th is may refl ect a strong dependence of cave communities on long term surface productivity (as refl ected in actual evapotranspiration), because the subterranean fauna relies almost entirely on resources produced outside caves. On a smaller scale, Zagmajster et al. (2008, 2010) analyzed the pattern of cave beetle species richness within the Dinarides, and found two hotspots – in to the north in Slovenia and one to the south in southern Serbia and Montenegro. Th eir analysis is especially noteworthy because it takes into account diff erent levels of collecting intensity, and provides an estimate of species richness independent of the diff erent levels of collecting. Culver & Sket (2000) (updated by Culver & Pipan 2013) took a diff erent approach to analyzing the geography, and studied, not regions, but individual high diversity caves. Currently there are nine karst caves and wells with more than 25 stygogiont species known and six karst caves and lava tubes with more than 25 troglobionts species known (Table 3). For stygobionts, a geographical component is evident. More than half of the caves are in the Dinarides. Th e Dinaric karst has two unique features – it is adjacent to the Mediterranean Sea and karst development as measured by cave passage density is higher than elsewhere. Adjacency to the Mediterranean aff orded opportunities for invasion of marine taxa during periods of drying, such as the Messinian salinity crisis. Th e remaining cases, with one exception, are entirely phreatic (permanent ground water) or with major phreatic components. Th e

eschweizerbart_xxx Karst environment 109 exception is Walsingham Cave in Bermuda, a high-energy anchialine cave with chemoautotrophic production. Th us, the mark of history is obvious with the predominance of examples from one geographic region – the Dinaric karst. Th e reason that phreatic habitats are so well represented is less clear but it maybe that the contiguous area of these aquifers is much greater than the contiguous areas of other aquatic subterranean habitats, or that chemoautotrophic production is occurring in permanent groundwater, resulting in greater availability of organic carbon and nutrient. Th e most striking aspect of the six caves with more than 25 troglobionts (Table 3) is that two are high productivity, long lava tubes in the Canary Islands. Among remaining karst caves, two are in the Dinarides, one is a chemoautotrophic cave with high productivity, and one is the longest cave in the world with over 500 km of passage – Mammoth Cave in Kentucky, USA. Th e Dinaric caves are in the ridge of high diversity described by Culver et al. (2006). Hence, both history and productivity may play a role in this pattern. Stygobiotic and troglobiotic species richness is typically lower in the tropics, but this is in part because guano specialists, species not found outside of caves, are not usually included in lists of troglobionts because they are typically neither eyeless nor depigmented (Deharveng & Bedos 2012, but see Culver & Pipan 2014). Overall diversity in tropical caves is high, with many non- obligate cave-dwellers utilizing caves. Deharveng & Bedos (2012) conclude the following:

Table 3. Caves with more than 25 stygobionts (A) or 25 troglobionts (B). From Culver & Pipan (2013).

Site name Country Number of species Region/ecology A. Stygobionts Postojna Planina Cave System Slovenia 48 Dinarides Vjetrenica Bosnia & Hercegovina 40 Dinarides Walsingham Cave Bermuda 37 Anchialine and chemoautotrphic Triadou Aquifer France 34 Phreatic Robe River Australia 32 Phreatic Križna jama Slovenia 29 Dinarides Logarček Slovenia 28 Dinarides Šica-Krka System Slovenia 27 Dinarides Edwards Aquifer Texas, USA 27 Phreatic B. TROGLOBIONTS Postojna Planina Cave System Slovenia 36 Dinarides Cueva de Felipe Reventón Canary Islands, Spain 36 Lava tube Vjetrenica Bosnia & Hercegovina 30 Dinarides Peştera Movile Romania 29 Chemoautotrophic Cueva del Viento1 Canary Islands, Spain 28 Lava tube Mammoth Kentucky, USA 26 Longest cave 1 Includes Cueva del Sobrado

eschweizerbart_xxx 110 D.C. Culver

• Richness in troglobionts or guanobionts is rarely very low in the tropics, and never null as in temperate regions aff ected by glaciations. • Th e terrestrial fauna appear to be more diverse, at least in well studied caves, in the Oriental and Australian regions than in the Neotropics or Africa. • Th e richest hotspot of the tropical subterranean fauna is the Maros karst in South Sulawesi. From these studies, we can tentatively conclude that important areas of cave biodiversity occur in many regions, but that the hotspot of biodiversity is the Dinaric Mountains, ranging from Italy and Slovenia in the north to Albania and Montenegro in the south. Tropical diversity is generally lower, but the tropics are also the site of signifi cant subterranean biodiversity. Th e causes for the lower diversity are not entirely clear, but it is unlikely to be primarily the result of lack of study, especially given the extensive work in tropical caves by Deharveng, Bedos, Peck, and others.

3 Fauna of shallow subterranean habitats

Th e fauna of shallow subterranean habitats is much less well studied than that of caves, and typically there are only a few sites where it has been studied. Hence, the geographic pattern of species richness is largely unknown.

3.1 Aquatic epikarst

Th e epikarst (Mangin 1973), or subcutaneous zone, is the uppermost part of karstifi ed rock, a perched aquifer, and an ecotone between surface and subterranean environments. It has been variously defi ned but in general it is the boundary between soil and rock in karst, honeycombed with small fractures and solution pockets. Its vertical extent varies from nearly zero to a few meters. Th e epikarst consists of a series of small cavities and crevices, some of which are water- fi lled, some of which are fi lled with organic material, humus, and insoluble material, and some of which are air-fi lled. While some components of the epikarst fauna are found in drip pools (Pipan et al. 2010), a more unbiased sample can be obtained by constant fi ltering of water dripping from the ceilings of cave passages. While epikarst can only be sampled in cave passages, its occurrence is much more continuous. A wide variety of invertebrate species are known primarily or exclusively from epikarst (Pipan 2005). In the compendium of subsurface aquatic species Stygofauna mundi (Botosaneanu 1986), over 10 species of oligochaetes, 280 species of crustaceans, 2 species of beetles, and 30 species of fl atworms are reported from percolating (epikarst) waters of caves. Eight genera of crustaceans have 10 or more species that are found in the epikarst. In North America, the amphipod Stygobromus and the isopod Caecidotea are common epikarst species, whereas in Europe the isopod Proasellus, the syncarid Iberobathynella, the cyclopoid copepods Speocyclops and Diacyclops, and the harpacticoid copepods Bryocamptus, Elaphoidella, and Parastenocaris predominate.

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Species richness in the epikarst is remarkably high and oft en rivals that found in cave streams. Table 4 summarizes what is known about copepod epikarst drip diversity in well sampled caves. Up to 16 species of stygobionts were found in one cave (Postojna Planina Cave System, also the richest known cave for stygobionts (Table 3)), and a minimum of two stygobionts and seven copepod species overall in a Romanian cave. Meleg et al. (2011) estimate that the total number of stygobionts in this cave is fi ve, if sampling were complete.

Table 4. Species richness of epikarst copepods in well sampled caves. Data from Culver & Pipan (2014).

Cave Country Number of Number of Copepod Stygobiotic Species Copepod Species Velika Pasica Slovenia 12 9 Postojna Planina Cave System Slovenia 23 16 Škocjanske jame Slovenia 17 10 Dimnice Slovenia 12 11 Županova jama Slovenia 16 14 Organ Cave West Virginia, USA 10 7 Peştera Vadu Crişului Romania 16 4 Peştera cu Apă din Valea Leşului Romania 7 3 Peştera Ciur Izbuc Romania 7 2

3.2 Terrestrial epikarst and other habitats of the milieu souterrain superfi ciel

Since many cavities in epikarst are air fi lled, it is not surprising that there is a terrestrial epikarst fauna. Th ere are other similar terrestrial habitats in karst, including talus slopes and regolith in general. Most collections of terrestrial epikarst (milieu souterrain superfi ciel) karst species have been by-catches from dripping water. MSS traps are available (see López & Oromí 2010), but little used in karst settings. Novak et al. (2012), as part of an extensive study of the fauna of small caves in northeast Slovenia, found a bimodal distribution of troglobionts with respect to depth below the surface (Fig. 2). Th e associated the shallower species (which were more numerous) with epikarst.

3.3 Calcrete aquifers

Calcrete aquifers are carbonate deposits, typically in desert terrains (Pentecost 2005). While widely occurring in desert areas throughout the world, the fauna has only been studied in the calcrete aquifers of the Pilbara and Yilgarn of Western Australia, and to a lesser extent in the Northern Territory.

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Calcrete aquifers in Austrialia are typically tens of km long but only 10 m or less thick Th ose in the Yilgarn are typically with 10 m of the surface, but those of the Pilbara are not. Th ey form during drying periods with high evaporation but also when there are periods of rare but concentrated rainfall. Formation is associated with salt lakes (playas, sebkras), and results from evaporation of carbonate rich water. Water in calcrete aquifers can have very high salinity, which may be a barrier to dispersal within the calcrete. According to Humphreys et al. (2009), the system is like an estuary, but is not tidal, and unconnected to any ocean.

Fig. 2. Comparative normalized spatial density map of 19 troglomorphic taxa in small caves in north central Slovenia. From Novak et al. (2012).

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Because of its long geological history, some of the fauna of calcrete aquifers is likely very ancient, part of the Gondwana and Tethys fauna. A classic example of a Gondwana component is the crustacean order Splaeogriphacea. All or nearly all stygobionts, whether ancient or modern in origin, are limited to a single calcrete aquifer or paleo-drainage. One group is specialized in the subterranean saline and hypersaline water near the playas – the isopod genus Haloniscus. A particularly rich and well studied component of the fauna are the diving beetles in the family Dytiscidae. Colonization of calcrete aquifers was the result of increased aridity, especially during the Pliocene. Th e restriction of nearly all species to a single calcrete aquifer, and the lack of relationship of species in adjacent aquifers, suggests that dispersal is rare. Th e occurrence of pairs and triplets of sister dytscid species is quite common, and evidence points to speciation within the aquifer, either micro-allopatric, parapatric, or sympatric. Even within an aquifer there is some geographic diff erentiation in a species, suggesting the possibility of cryptic speciation. Overall, species richness is high, and calcrete aquifers are gobally important sites of subterranean biodiversity. Indi- vidual aquifers have reported to have up to 17 stygobiotic species (Humphreys et al. 2009).

4 Biota of photic habitats in karst

Karst topography can have a profound eff ect on the biota. Th is eff ect is clearly recognized in some countries, such as Croatia and Slovenia, where phytosociologists and other botanists recognize karst terrains as unique. Th ere is also a special wetlands type in Ireland and perhaps elsewhere – turloughs – that are a type of temporary lake and karst feature with a unique set of communities (Sheehy Skeffington et al. 2006, Sheehy Skeffington & Gormally 2007). Wetlands that occur in the interior of karst areas (poljes, uvalas, intermittent lakes, karst pans, etc.) are uncommon but important in a variety of ways, including stopovers for migratory birds and sites of unique plant communities (Pipan & Culver 2012b). Many of these interior karst wetlands are connected to groundwater via estavelles.

4.1 Th in soils – “barrens”

Among the eff ects of karst landscapes are the inversion of altitudinal gradients in deep dolines in alpine regions (Surina 2005). Th e bottom of dolinas had vegetation characteristic of higher elevations. Karst landscapes have eff ects on vegetation in non-mountainous terrains as well. For example, there are climatic, soil, and vegetation gradients in large plateau sinkholes in France (Bayonet 1998). In many karst areas, thin soils develop, especially at the tops of sinkholes and dolinas. In the fl at-bedded karst regions of the central United States (the Interior Low Plateaus), such areas, called “cedar glades”, without a full canopy of trees and dominated by eastern red cedar (Juniperus virginiana) have a unique vegetation characterized by drought resistant plants (Baskin & Baskin 2003). A number of the species of cedar glades are at risk because of the relative rarity of the habitat.

eschweizerbart_xxx 114 D.C. Culver

4.2 Cave entrances and other rock faces

Many organisms, not just animals but plants and algae as well, are typically or even exclusively found around cave entrances. Th ese are not organisms of aphotic, true subterranean environments, but rather inhabitants of dimly lit twilight zones. Several species of birds nest near entrances or in shallow aphotic zones in caves. One of the most interesting is the oilbird (guacharo), Steatornis caripensis , found in caves in Trinidad and northwestern South America, where colonies can be as large as 5000 individuals. A fruit-eater, this large bird, with a wingspan of 1 m, nests in caves and cave entrances, has a major impact on seed dispersal in the surrounding forest (Thomas et al.1993). A variety of other species can be found in the entrance zone. Some are there to escape summer heat and some are there to avoid predators, but some are entrance-zone specialists, oft en predators of the animals coming into the entrance. Th e North American cave salamander, Eurycea lucifuga is really misnamed since it is more common around entrances than deep in the cave (Camp & Jensen 2007). Invertebrate predators commonly found in cave entrances in Europe and North America are web-building spiders in the genus Meta. Th e sticky webs of the rather large European M. menardi and American M. ovalis are almost always within the limits of daylight penetration and in the path of fl ying insects. Little is known about mosses, lichens, and ferns in caves. It is a common observation that the rock around cave entrances oft en has a rich moss and fern fl ora. For example, Dobat (1998) reported that over half of the cave entrances in Jura Mountains of France had the moss Th amnobryum alopecurum. Cave entrances are oft en known for their rich growth of ferns. Descriptions of tropical caves oft en mention the profusion of ferns at the entrance, and several caves in the United States and Great Britain are known as Fern Cave. Most of ferns and mosses around cave entrances are classifi ed as calcicoles, or calcium-loving, and it is unlikely that they are specialized for low light. However, in some situations cave entrances are more than just a slab of wet limestone from the point of view of ferns. Th e American Hart’s Tongue Fern, Asple- nium scolopendrium var. americanum is rather common in Canada, but rare in the United States where it is listed as a threatened species under the US Endangered Species Act. It occasionally occurs in northern Michigan and New York on carbonate rock. Th e only other known sites are nearly 1000 km to the south around the entrances to three vertical pits in Tennessee and Alabama (Evans 1982). It seems very likely that the summertime moist, cool temperatures around the pit allow this northern species to survive in southern locations.

5 Karst habitats as permanent and temporary climate refuges

It is well accepted that many species become isolated in caves to escape the vicissitudes of climate in surface habitats, and this theory is called the Climate Relict Hypothesis (Culver & Pipan 2009). But karst features, especially terrestrial epikarst (and other MSS habitats) as well as vertical pits open to the surface, show a pattern of truncation of the extremes of temperature. It is the extremes rather than overall variability that is reduced. Pipan et al. (2011) and Culver & Pipan (2013) provide a number of examples of this eff ect in the MSS, both in karst and non-karst areas. Th is is an area sorely in need of more research.

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Acknowledgements

Many of the ideas expressed here were developed in collaboration with Tanja Pipan. Some of the material is modifi ed from our books (Culver & Pipan 2009, 2014).

References

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Author’s address: David C. Culver, Department of Environmental Science, American University, 4400 Massachusetts Ave. NW, Washington, D.C., U.S.A., 20016. e-mail: [email protected]

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